Consequences of acute and long-term removal of neuromodulatory input on the episodic gastric rhythm of the crabCancer borealis

Abstract

Hamood AW, Marder E. Consequences of acute and long-term removal of neuromodulatory input on the episodic gastric rhythm of the crab Cancer borealis. J Neurophysiol 114: 1677-1692. First published July 8, 2015 doi:10.1152/jn.00536.2015.-For decades, the episodic gastric rhythm of the crustacean stomatogastric nervous system (STNS) has served as an important model system for understanding the generation of rhythmic motor behaviors. Here we quantitatively describe many features of the gastric rhythm of the crab Cancer borealis under several conditions. First, we analyzed spontaneous gastric rhythms produced by freshly dissected preparations of the STNS, including the cycle frequency and phase relationships among gastric units. We find that phase is relatively conserved across frequency, similar to the pyloric rhythm. We also describe relationships between these two rhythms, including a significant gastric/ pyloric frequency correlation. We then performed continuous, dayslong extracellular recordings of gastric activity from preparations of the STNS in which neuromodulatory inputs to the stomatogastric ganglion were left intact and also from preparations in which these modulatory inputs were cut (decentralization). This allowed us to provide quantitative descriptions of variability and phase conservation within preparations across time. For intact preparations, gastric activity was more variable than pyloric activity but remained relatively stable across 4 -6 days, and many significant correlations were found between phase and frequency within animals. Decentralized preparations displayed fewer episodes of gastric activity, with altered phase relationships, lower frequencies, and reduced coordination both among gastric units and between the gastric and pyloric rhythms. Together, these results provide insight into the role of neuromodulation in episodic pattern generation and the extent of animal-to-animal variability in features of spontaneously occurring gastric rhythms.

Molecular mechanisms of homeostatic plasticity in central pattern generator networks

“…Future work will more precisely dissect the signaling pathways and regulatory targets that result in feedback across levels of function, from transcription to posttranslational modification. Furthermore, subsequent work is needed at the molecular level to better understand the role of individual variability both in the differences in response to potentially destabilizing changes in feedback (Hamood, Haddad, Otopalik, Rosenbaum, & Marder, ; Hamood & Marder, ), as well as the role of compensatory plasticity as a source of individual variability in expression of channels and receptors that are related to neuronal output (e.g., see our discussion of this in Schulz & Lane, ). By better understanding how neurons and networks balance ongoing activity and feedback regulation, we will gain a better understanding not only of some of the most fundamental principles underlying network robustness, but also how aberrant actions of these pathways may contribute to network failure and pathology.…”

Output variability across animals and levels in a motor system

“…Variances are reported from the gastric pattern in the isolated crab STNS within animals but this is convolved across episodes over many days ( Hamood and Marder, 2015 ). In this episodic motor pattern, cycle-to-cycle variabilities were substantially larger than those in the ongoing leech heartbeat CPG pattern and motor pattern.…”

“…But how constant is network output across individuals? Not very seems to be the answer when looking at the literature more closely (e.g., locomotion in mice [ Bellardita and Kiehn, 2015 ] and zebrafish [ Masino and Fetcho, 2005 ; Wiggin et al, 2014 ]; food processing in crabs [ Hamood et al, 2015 ; Hamood and Marder, 2015 ; Yarger and Stein, 2015 ], crawling in fly larvae [ Pulver et al, 2015 ]).…”

The complexity of small circuits: the stomatogastric nervous system

“…Over the course of tens of hours, circuit properties are then reconfigured. Such reconfiguration can be sufficient to recover pyloric activity [54,55], but more recent work shows that short of recovery, long-term removal of neuromodulators and subsequent changes in circuit components increases variability of both pyloric and gastric mill activity [56,57]. Removal of neuromodulation also causes changes severe enough to prevent functional activity when inputs are restored [58].…”